ARGONAUTE9-dependent Silencing of Transposable Elements in Pericentromeric Regions of Arabidopsis

Overview

Journal Plant Signal Behav

Specialty Biology

Date 2010 Nov 9

PMID 21057207

Citations 24

Authors

Noe Duran-Figueroa

Jean-Philippe Vielle-Calzada

Affiliations

Soon will be listed here.

Abstract

Recent evidence indicates that the establishment of the haploid phase of the plant life cycle requires epigenetic mechanisms that control reproductive cell fate. We previously showed that in Arabidopsis thaliana (Arabidopsis) mutations in ARGONAUTE9 (AGO9) result in defective cell specification during megasporogenesis. AGO9 preferentially interacts with 24 nucleotide (nt) small RNAs (sRNAs) derived from transposable elements (TEs), and its sporophytic activity is required to silence TEs in the female gametophyte. Here we show that AGO9 can bind in vitro to 24 nt sRNAs corresponding to Athila retrotransposons expressed in the ovule prior to pollination. We also show that AGO9 is necessary to inactivate a significant proportion of long terminal repeat retrotransposons (LTRs) in the ovule, and that its predominant TE targets are located in the pericentromeric regions of all 5 chromosomes, suggesting a link between the AGO9-dependent sRNA pathway and heterochromatin formation. Our extended results point towards the existence of a tissue-specific mechanism of sRNA-dependent TE silencing in the ovule.

Citing Articles

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References

Teixeira F, Colot V . Repeat elements and the Arabidopsis DNA methylation landscape. Heredity (Edinb). 2010; 105(1):14-23. DOI: 10.1038/hdy.2010.52. View

Mi S, Cai T, Hu Y, Chen Y, Hodges E, Ni F . Sorting of small RNAs into Arabidopsis argonaute complexes is directed by the 5' terminal nucleotide. Cell. 2008; 133(1):116-27. PMC: 2981139. DOI: 10.1016/j.cell.2008.02.034. View

Hosouchi T, Kumekawa N, Tsuruoka H, Kotani H . Physical map-based sizes of the centromeric regions of Arabidopsis thaliana chromosomes 1, 2, and 3. DNA Res. 2002; 9(4):117-21. DOI: 10.1093/dnares/9.4.117. View

Yang W, Shi D, Chen Y . Female gametophyte development in flowering plants. Annu Rev Plant Biol. 2010; 61:89-108. DOI: 10.1146/annurev-arplant-042809-112203. View

Walbot V, Evans M . Unique features of the plant life cycle and their consequences. Nat Rev Genet. 2003; 4(5):369-79. DOI: 10.1038/nrg1064. View

Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D . Circos: an information aesthetic for comparative genomics. Genome Res. 2009; 19(9):1639-45. PMC: 2752132. DOI: 10.1101/gr.092759.109. View

Mosher R, Melnyk C, Kelly K, Dunn R, Studholme D, Baulcombe D . Uniparental expression of PolIV-dependent siRNAs in developing endosperm of Arabidopsis. Nature. 2009; 460(7252):283-6. DOI: 10.1038/nature08084. View

Slotkin R, Vaughn M, Borges F, Tanurdzic M, Becker J, Feijo J . Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell. 2009; 136(3):461-72. PMC: 2661848. DOI: 10.1016/j.cell.2008.12.038. View

Havecker E, Wallbridge L, Hardcastle T, Bush M, Kelly K, Dunn R . The Arabidopsis RNA-directed DNA methylation argonautes functionally diverge based on their expression and interaction with target loci. Plant Cell. 2010; 22(2):321-34. PMC: 2845420. DOI: 10.1105/tpc.109.072199. View

10.

Mosher R, Schwach F, Studholme D, Baulcombe D . PolIVb influences RNA-directed DNA methylation independently of its role in siRNA biogenesis. Proc Natl Acad Sci U S A. 2008; 105(8):3145-50. PMC: 2268599. DOI: 10.1073/pnas.0709632105. View

11.

Pall G, Hamilton A . Improved northern blot method for enhanced detection of small RNA. Nat Protoc. 2008; 3(6):1077-84. DOI: 10.1038/nprot.2008.67. View

12.

Wu M, Tian Q, Reed J . Arabidopsis microRNA167 controls patterns of ARF6 and ARF8 expression, and regulates both female and male reproduction. Development. 2006; 133(21):4211-8. DOI: 10.1242/dev.02602. View

13.

Olmedo-Monfil V, Duran-Figueroa N, Arteaga-Vazquez M, Demesa-Arevalo E, Autran D, Grimanelli D . Control of female gamete formation by a small RNA pathway in Arabidopsis. Nature. 2010; 464(7288):628-32. PMC: 4613780. DOI: 10.1038/nature08828. View

14.

Vazquez F, Legrand S, Windels D . The biosynthetic pathways and biological scopes of plant small RNAs. Trends Plant Sci. 2010; 15(6):337-45. DOI: 10.1016/j.tplants.2010.04.001. View

15.

Mosher R, Melnyk C . siRNAs and DNA methylation: seedy epigenetics. Trends Plant Sci. 2010; 15(4):204-10. DOI: 10.1016/j.tplants.2010.01.002. View

16.

Henderson I, Jacobsen S . Epigenetic inheritance in plants. Nature. 2007; 447(7143):418-24. DOI: 10.1038/nature05917. View